Plasticity in the Central Nervous System

Learning and Memory

James L. McGaugh, Federico Berm£dez-Rattoni, Roberto A. Prado-Alcal, Roberto A. Prado-Alcala

• Publisher: Routledge
• Year: 2019
• ISBN:
  9781317729013
• Edition: 1
• Topic: Psicologia
• Subtopic: Neuropsicologia

Catalyzed by the development of new neurobiological and behavioral techniques as well as new conceptual and theoretical approaches to the study of the relationship between brain and behavior, research exploring brain functions enabling learning and memory has greatly accelerated in recent years. The chapters in this book reflect current theoretical approaches to the study of brain and memory and provide new insights concerning the cellular bases of memory and the differential involvement of brain systems in different forms of memory. By presenting up-to-date summaries of research investigating brain mechanisms underlying learning and memory, these chapters help to place current findings in appropriate theoretical context, and further stimulate research inquiry attempting to understand how the brain makes memory. Divided into three sections, coverage in this volume includes:
* a discussion of pharmacological approaches to the study of brain and memory;
* a review of experiments using a variety of techniques, including brain lesions, brain grafting, and electrophysiological recording to investigate the role of different brain regions in learning and memory; and
* an examination of molecular analyses of events associated with memory formation.

1 Brain and Behavior: Bridging the Barranca

John Garcia

University of California, Los Angeles

In point of fact only one thing in life is of actual interest for us—our psychical experience. But its mechanism has been and still remains wrapped in mystery. All human resources—art, religion, literature, philosophy, and historical science—have combined to throw light on this darkness. Man has at his disposal yet another powerful resource—natural science with its strictly objective methods.

—Pavlov (1904)

So spoke I. P. Pavlov in 1904 at Stockholm in the final paragraph of his Nobel Prize address introducing classical conditioning as a new method for studying mind by precisely controlling learned behavior and noting the concomitant neural activity (Kaplan, pp. 56–57). Following Pavlov, scientists have concentrated on either the peripheral or central aspects of the behaving animal, and generally shunned the mind and its vagaries. As a result, there are two great mountain ranges of literature, one on behavioral research and the other on brain research, with a huge chasm, or barranca, separating them. Buried at the bottom of the barranca lies the unifying concept of mind.

The mind baffles us because none of us has direct access to the mind of another human. Quite simply, we have direct access to our own minds and we know that we conceal and disguise our own thoughts and motives, presenting a false front to others, so we are certain that others lie to us as well. Great effort is expended in detecting lies and extracting the truth from others, but no one has come up with a foolproof method.

We behavioral neuroscientists, whose occupation title reflects the barranca, need to keep a constructive attitude toward mind. Building sure bridges across the behavior-brain barranca and illuminating it with strictly objective methods what Pavlov called our psychical experience is the essential task of behavioral neuroscience. Whether it is fair or not, our research will ultimately be judged according to how much light we shed on that singular enigma called mind. For our task, the adjective behavioral is overly restrictive; we should be known for what we are, mental neuroscientists.

I suggest to start that we accept mind as a causal agent. Curiously, abnormal brains and deranged minds are generally accepted as causes of aberrant behavior, whereas sound brains and normal minds are suspect. Second, we should give up the absolutist position that we must have direct access to other minds. It is an illusory shibboleth; most scientific principles based on indirect inferences. Third, I suggest we get on with our job of locating the mind and the organized brain mechanisms it uses for controlling behavior.

The foundations of mental neuroscience were laid down over three centuries ago. Nevertheless, how we project minds onto other organisms still raises epistemological issues and endless arguments. I cannot define exactly the kind of brain organization we’re looking for, because mind must be defined only by future empirical research. For now I can only provide you this basic axiom:

Mind is a manifestation whose validity is a function of its locus, such that no amount of evidence can disprove its existence in me and you, or prove its existence in them out there.

THE LANGUAGE BARRANCA

Historically, scientists turned their backs on the barranca, choosing either behavior or the brain, and over the centuries developed two objective languages with little or no functional relevance to each other.

On one side, the language developed by behavioral psychologists is in a constant state of flux, so that each new generation scarcely understands what the older generation was talking about. Behavioral theorists speak of stimulus and response, by which they mean cause and effect. When looking at any two events in a reliable behavioral sequence, the first event is the stimulus and the second event is the response, but the second event is also a stimulus for subsequent events. Furthermore, each response generates internal feedback stimuli, and thus a cascade of responses. The only way to clear up this muddle is to specify the afferent and efferent paths involved, but such specificity is viewed as a reductionistic and physicalistic surrender of liberated psychology to imperial biology. Still that’s better than a flight into the lofty abstractions of logical models and mathematics preferred by some theorists of pure behavior and pure cognition.

On the other side of the barranca, the neuroanatomists developed a language to describe the brain that is stable, concrete, and archaic. Their language emphasizes the form and structure of landmarks in the brain without much regard for their functions, resulting in a colorful melange that is very difficult for students to memorize. The cerebrum is described as some strange fruit marked by a deep fissure running fore and aft and wrapped in two mothers, one tough and the other tender. It sits atop a stem with a little cerebrum attached directly below and to the rear. The interior of the brain is filled with a wondrous mix of rooms, hollows, tracts, bodies, nets, sea horses, almonds, worms, teats and tails, organized so that there is one of everything down the middle and two of everything down the sides.

Given the infinite human capacity to generate neologisms, metaphors, and translations, these semantic problems will clear up naturally as research progresses. As I will point out further, the attempt to establish permanent definitions and logical schemes has interfered with empirical research in mental neuroscience.

MICHELLE AND HERMISSENDA

Let us first contemplate the awesome size of the barranca as portrayed by Alkon (1992) in his book, Memory’s Voice: Deciphering the Mind Brain Code. Alkon interlaces a sensitive psychiatric case history of a childhood friend, Michelle, with his search for fundamental brain mechanisms of learning and memory in the sea slug, Hermissenda. He does so with insight and literary skill, but covering over the barranca with a seamless tapestry of plausibility concealing the enormous task of closure before those who stand on either one precipice pr the other.

Michelle grew up under an oppressive violent father, who used his overwhelming power to beat his little girl savagely and belittle her psychologically. As a child, unable to escape the pain and humiliation, she tried to be good, but was only rewarded with more punishment. As an adolescent, she strove for perfection, but was met with contempt and abuse. As a beautiful, talented young woman, she finally broke free of her tormentor in an emotional explosion, but she was never free of the coping mechanisms engraved on her mind during development, and thus, memory became her tormentor. Her fate led her through feelings of guilt and futility, to alcoholism and suicide. In a time when it is fashionable to attribute such problems to heredity, Alkon reminds us that a normal, healthy human can be incapacitated by residual memories of a hostile environment. Such enduring memories, incorporating species-specific emotions and motor patterns modified by personal experience, must reflect a complex mental system pervading the central nervous system.

Hermissenda, the Pacific sea snail also has its problems, but it lives in a world far different from Michelle’s. About 3cm in length and gracefully slender, it explores the movements and chemicals in its watery environment with a crown of tentacles and wears a coat of featherlike appendages that increase its diffusion surface for respiration and elimination. It clings to the substrate with a muscular foot resisting currents threatening to overturn it as it creeps along the sea floor.

After studying a number of organisms, Alkon selected Hermissenda because of its relatively simple nervous system. He explored its receptors and traced its nervous pathways for years until he had comprehensive wiring diagrams for its visual system, optic ganglia, and vestibular system, including the interactions of these structures with the right and left side of the snail’s brain. Employing Pavlov’s general strategy, Alkon selected a visual conditioned signal (CS) and bodily rotation as the unconditioned stimulus (US); two events that are not likely to be coincidental in the natural world of the sea snail. He then traced the flow of signals through the nervous system and noted the changes occurring as a result of light-rotation pairing, establishing the acquisition and retention of a new association in the brain.

This is excellent research, and if he specifies how Hermissenda learns and remembers in a complete and convincing manner, Alkon deserves the highest accolades of science. But, he will have to go beyond the mechanisms by which cells live and communicate with each other, to reveal the entire mental structure by which Hermissenda learns and remembers how to cope with turbulence in its world, before we can see how Hermissenda relates to Michelle and her turbulent world. A maelstrom of change occurred as the two species diverged and adapted to vastly different environments. Some features were modified, some were lost and some were gained. However, there is the implicit assumption, perhaps unwarranted, that the basic circuitry remained relatively stable for eons so that the basics of human mind can be found in an invertebrate.

SEARCHING FOR NEUROBEHAVIORAL UNITS

Following four centuries of discourses on the associative mind by the empirical philosophers, Pavlov brought the association of ideas into the objective reality of a dog in the laboratory. He conditionally paired an auditory stimulus (S) eliciting the orienting response (R) with a gustatory S evoking a salivary R. After training a dog to salivate at the sound of the auditory S, Pavlov concluded that a new connection had been established between the auditory system and the salivary system in the dog’s brain.

Pavlov emphasized that in observing the conditioned salivary reflex he was studying the mind of the dog. The saliva exquisitely matched the nature of the oral stimulation and the expectations of the animal, ranging from a thin fluid for flushing sand out of the mouth to a slick mucin for lubricating dry food. Pavlov wrote, “We see here facts which are exact and constant and which seem to imply intelligence. But the entire mechanism of this intelligence is plain? (Kaplan, pp. 61–62).

As soon as Pavlov presented his classic paradigm, Thorndike offered a variant known as instrumental conditioning. Rather than an auditory S, Thorndike followed by a movement (R) executed by a hungry cat with food to elicit eating (R). He thought of conditioning in terms of R-R connections between associated responses and he specified that the arbiters of responses, rewards and punishments were the neurons of the brain. S-S and R-R conditioning paradigms remain the most popular neurobehavioral manipulations to this day because of the repetitive numerical data they generate. But that may be their greatest weakness. Learning may come from a sudden insight, an all-or-none process without practice. If so, a one-trial procedure may be more appropriate.

Of all the American learning theorists, Hull (1943) followed Pavlov most faithfully. Hull chose not to work on the neural connections himself, but rather, he postulated intervening neural events from behavioral data to guide the work of others working on the brain. Hull’s hypothetical postulates, couched in neurological terms, resided in the brain and were anchored to inputs (S) by afferent neural interaction and to outputs (R) by variations in excitatory and inhibitory reaction potentials. These input and output vagaries made Hull’s theory difficult to falsify. His ultimate goal was to establish the S-R connection as the basic unit of behavior.

As Hull’s system evolved, it became more behavioral and less neural, until Spence (1947), the dominant Hullian advocate of the time, abandoned the brain, saying, “… psychologists have come to realize that the explanation of behavioral events does not necessarily involve reduction to its physiological determinants.” Meanwhile, Skinner (1938) excoriated the mind, along with S-S conditioning. Claiming he had the natural unit of behavior, Skinner took over R-R conditioning, renaming it operant conditioning. Manipulating the behavior of hungry pigeons with food rewards, he tried to persuade us that human behavior follows the same laws and is essentially mindless.

The problem with Skinner’s denial is that the broad view of pigeons doing their own thing creates a suspicion that pigeons, like humans, have species-specific minds. That is true for almost any organism we come to know intimately. Jay B. Best once remarked to me, “The more I look at a flatworm, the more it seems to be a human in a flatworm suit.” That may explain why after years of looking at insects, entomologists Kinsey (Kinsey, Pomeroy, & Martin, 1948) and Wilson (1975) suddenly turned their attention to human social behavior and made a great impact on psychology.

The issue facing the mental neuroscientist is similar to that faced by the S-R behaviorists in search of the unit of conditioning. Can learning and memory be adequately explained by unitary elements such as changes in a neuron, or in a synapse, or in the formation of a protein? I once heard Eric Kandel make a dismal prediction that learning may be accomplished by the “housekeeping activities” of neurons. If so, the goal of neuroscience is to describe the complex circuitry of neurons supporting holistic mind-systems.

Skinner’s Radical Behaviorism

Skinner (1989, 1990) was the most prominent and most adamant proponent of mindless behaviorism. He was articulate but directed his argument towards an archaic view of mind that no scientist holds today. In 1989, he drew from his background as a college English major to argue that mentalistic terms spring from behavioristic roots. To say that thinking is a form of operant responding under the control of environmental contingencies is not an answer. It is simply a restatement of Freud’s basic question, “What good comes to this patient from these thoughts?”

In 1990 Skinner accepted natural selection of species morphology and species behavior, but he cuts a piece of the evolutionary action out for himself. Natural selection, he said, “… prepares a species only for a future that resembles the past.” That fault is corrected by a “second type” of evolution, namely, “operant conditioning, through which variations in the behavior of the individual are selected by features of the environment that are not stable enough to play any part in evolution.”

Of course, unstable features play an evolutionary role by selecting individuals who learn and remember how to cope with such unstableness. That was fully discussed by Darwin and the evolutionists before and after him (Garcia y Robertson & Garcia, 1987). Some of the individuals who could learn and remember arrived in Skinner’s laboratory in the form of pigeons prepared by natural selection to deal with the unstableness in his operant feeding schedules. Skinner (1990) did not discuss the contributions of evolutionary adaptation to conditioned responses, as Pavlov did, and that proved to be the source of his errors, tending to bury important variables in a singular concept. For example, reinforcement is vital to operant conditioning, but many reinforcers are species-specific or response-specific, and such specificity was not stressed even in the pigeon.

The pigeon, like other organisms, cannot deal with changes falling outside the range of unstableness found in its evolutionary niche. In nature the hungry pigeon searches for a seed that provides the target to peck, the signal to peck, and the reinforcement to peck in one convenient package. In the Skinner box, if these three features were presented together approximating the evolutionary condition, the pigeon performed well; but if they were spread far apart, the pigeon failed at arrangements that other species handle with ease. The pigeons’s failure tells us something about the pigeon’s mind and brain: Apparently when looking for seeds, the pigeon must catch all three features in a single glance, just as did its ancestors (Garcia & Garcia y Robertson, 1985).

Mental neuroscientists can profit by studying Skinner’s mistakes. Subjects must be selected and studied with care, so must their adaptive behavioral functions. For certain functions, a wide variety of organisms may serve as subjects. For example, toxiphobic conditioning has been profitably studied in a wide range of vertebrate and invertebrate species, from primates to mollusks. However, even under the threat of poison, human behavior is a poor analogue for the wide range of snail behaviors, as under starvation, pigeon behaviors are poor analogues for human behaviors. Research on any given function in any one species can serve as a preliminary step to research in another species only when structural homologies underlying the given behavioral function are understood in terms of comparative anatomy and adaptive evolution. In toxiphobic conditioning, those homologies reside in the neural controls of ingestion and gut common to so many species. Beginnings toward that end have been made in the snail (Gelperin, Chang, & Reingold, 1978) and the rat (Garcia, Lasiter, Bermudez-Rattoni, & Deems, 1985).

Cognitive Maps and Animal Minds

Fortunately, the mind was kept alive and well by Tolman, who was also studying the behavior of rats in mazes. Tolman (1951) discussed concepts such as purpose, cognition, and the behavioristic theory of ideas. He described the vacillation of the rat at a choice point just before it switched to the correct path and wrote “whenever an org...

Table of contents

• Cover
• Half Title
• Title Page
• Copyright Page
• Table of Contents
• Preface
• 1. Brain and Behavior: Bridging the Barranca
• 2. Involvement of the Amygdala in the Regulation of Memory Storage
• 3. Role of the Hippocampus, Amygdala, and Entorhinal Cortex In Memory Storage and Expression
• 4. Serial and Parallel Processing During Memory Consolidation
• 5. The Role of the Insular Cortex in the Acquisition and Long Lasing Memory for Aversively Motivated Behavior
• 6. Somatic Gene Transfer to the Brain: A Tool to Study the Necessary and Sufficient Structure/Function Requirements for Learning and Memory
• 7. Reversible Lesions Reveal Hidden Stages of Learning
• 8. Cerebellar Localization of a Memory Trace
• 9. Persistent Questions About Hippocampal Function in Memory
• 10. Frontal Cortex and the Cognitive Support of Behavior
• 11. Correlates of Taste and Taste-Aversion Learning in the Rodent Brain
• 12. Time-Dependent Biochemical and Cellular Processes in Memory Formation
• Author Index
• Subject Index